Rates Of Extra-pair Paternity Research Articles

Male decisions or female accessibility? Spatiotemporal patterns of extra pair paternity in a songbird

Extra pair paternity is widespread in birds, but its high variability across years, populations, and species is to a great extent unresolved. Here we explored, during 2 breeding seasons, population and individual accessibility to fertile females at different spatiotemporal scales in a population of pied flycatchers (Ficedula hypoleuca) to understand whether individual patterns of extra pair paternity were due to adaptive individual behavior or ecological constraints. Our aim was to comprehend variation in extra pair paternity population patterns through the understanding of individual behavior. At the population level, extra pair paternity probability decayed with distance between nests. At the individual level, however, males engaged in extra pair paternity with distant (up to 390 m) females despite the fact that there were often fertile females in closer territories. Extra pair paternity cases occurred mostly during egg laying and the incubation of the extra pair male’s social female despite that other neighboring females were fertile before and after these periods. Results suggest a male strategy to maximize reproductive output by guarding their social females during their peak of fertility, seeking extra pair paternity afterwards and investing in parental duties once their social nestlings hatch. This may explain why extra pair paternity rate was higher in the year with lower breeding synchrony, because this allowed early-breeding males to have more extra pair paternity opportunities after their social mate laying onset. This study highlights the necessity of considering the social contexts of individuals at the spatiotemporal scales at which extra pair paternity takes place to understand variation in extra pair paternity patterns at the individual and population levels.

No evidence of extra-pair paternity or intraspecific brood parasitism in the Imperial Shag Phalacrocorax atriceps

In long-lived birds with significant paternal care contribution, as the case of seabirds, extra-pair paternity (EPP) is an infrequent phenomenon. Intriguingly, and in contrast to the general pattern exhibited by seabirds, EPP rates appear relatively high in the two species of cormorants and shags (Phalacrocoracidae family) analyzed so far. We test for EPP in the Imperial Shag Phalacrocorax atriceps, a medium-sized colonial seabird, using four DNA microsatellites originally developed for Great Cormorants P. carbo, and successfully cross-amplified in our focal species. We assessed the parentage of 110 chicks from 37 broods sampled at Punta Leon, Argentina, during the 2004 and 2005 breeding seasons. We found no evidence of EPP or intraspecific brood parasitism (IBP). Given our sample sizes, the upper 95% confidence limits for both EPP and IBP were estimated at 3.3% for the chicks and 8.4% for the broods. Our results did not agree with the previous reports of EPP within the family, probably as consequence of different copulation and courtship behaviours, mostly related to male’s solicitation display and females active search for extra pair copulations.

Who initiates extrapair mating in song sparrows?

Extrapair paternity (EPP) is a common feature of many mating systems. Although molecular methods have made it possible to document the rate of EPP across numerous taxa, we still lack an understanding of how and why EPP happens. Behavioral data on mating interactions are needed to answer this question. We employed radiotelemetry to follow the movement patterns of tagged song sparrows (Melospiza melodia) during their nesting cycle. We found that females and males commonly forayed onto neighboring territories in the prefertile period, frequently together. In the fertile period, however, the foray rate dropped significantly, and females largely stayed on their own territories. Concurrently in the fertile period, both the time mates spent in proximity and intrusion rates on their territories increased compared with the prefertile period. After the female started laying eggs, proximity of the mates to one another declined again, and some males started to foray onto neighboring territories, in most cases into territories where there was a fertile female. Thus, females do not seem to seek out particular males for extrapair copulations (EPCs) in their fertile period, but rather it is the males who actively seek extrapair mating. Males therefore face a trade-off between ensuring paternity at home and pursuing copulations elsewhere. Agonistic interactions between extrapair males and females were almost entirely absent, suggesting that males do not force females into copulations. Therefore, in song sparrows, males have to initiate EPCs by seeking out fertile females, suggesting that males probably drive the pattern of EPP in our

Infrequent Extra-Pair Paternity in the Banded Wren, a Synchronously Breeding Tropical Passerine

Abstract. Many species of socially monogamous birds engage in extra-pair copulations, but the extent of extra-pair paternity varies considerably by species. The ecological conditions contributing to interspecific variation in rates of extra-pair paternity remain unclear. We used a combination of single-nucleotide polymorphisms and microsatellites to document extra-pair paternity in the Banded Wren (Thryothorus pleurostictus), a socially monogamous neotropical passerine that lives in a highly seasonal environment. The rate of extra-pair paternity was relatively low, with extra-pair males siring 4% of offspring in 10% of nests. This low rate is consistent with current hypotheses predicting low rates of extra-pair paternity in nonmigratory species in which survivorship of adults is high, and it is contrary to the pattern predicted by hypotheses linking synchronous breeding with high rates of extra-pair paternity. Extra-pair males sang better and were more genetically similar to females than the males they cu...

Female choice and extra-pair paternity in a traditional human population

Seeking out extra-pair paternity (EPP) is a viable reproductive strategy for females in many pair-bonded species. Across human societies, women commonly engage in extra-marital affairs, suggesting this strategy may also be an important part of women's reproductive decision-making. Here, I show that among the Himba 17 per cent of all recorded marital births are attributed by women to EPP, and EPP is associated with significant increases in women's reproductive success. In contrast, there are no cases of EPP among children born into 'love match' marriages. This rate of EPP is higher than has been recorded in any other small-scale society. These results illustrate the importance of seeking EPP as a mechanism of female choice in humans, while simultaneously showing it to be highly variable and context-dependent.

Genetic Parentage and Local Population Structure in the Socially Monogamous Upland Sandpiper

Abstract. For a single lineage of birds, the diversity of mating systems and parental care among shorebirds (Charadrii) is high, which has made them an important group for investigations of the evolution of social mating systems. From 2003 to 2007, we studied a population of the Upland Sandpiper (Bartramia longicauda) at Konza Prairie Biological Station in northeastern Kansas. Our objectives were to determine the genetic mating system of this socially monogamous shorebird and to determine whether spatial patterns of philopatry and nest placement might affect opportunities for extra-pair mating. We used six microsatellite markers to estimate rates of extra-pair paternity in 58 family groups (107 parents, 184 offspring). We found that 30% of broods contained extra-pair offspring, representing 15% of chicks, the highest rate of extra-pair paternity ever reported in a socially monogamous shorebird. High rates of extra-pair paternity were not due to the degree of relatedness between partners in mated pairs, an...

Quantitative genetics and fitness consequences of neophilia in zebra finches

Consistent between-individual differences in context-general behavioral traits (often called personality traits) are particularly interesting for behavioral ecologists because they might show unexpected cross-context correlations and explain maladaptive behavior. In order to understand their evolutionary significance, it is relevant to know the heritability of these traits and how they relate to reproductive success. This might give insights into selective processes that maintain variation as well as into potential trade-offs. We scored approach to novel objects of 530 captive zebra finches in a familiar environment. Scores were highly repeatable and showed substantial additive genetic variation. We measured reproductive success, promiscuity, and extrapair paternity rates under aviary conditions and calculated linear and nonlinear selection differentials based on fertilization success as well as effects on chick-rearing success of pairs. Approach to novel objects had little influence on these components of reproductive success. However, we found that the social environment (manipulated operational sex ratios) influenced the correlation between approach to a novel object and the proportion of extrapair paternity. We also found that the sex ratio manipulation affected measures of the intensity of sexual selection. Both effects were stronger in males than in females. We conclude that despite the lack of differences in overall reproductive success, approach to novel objects reflects variation in reproductive strategies. Key words: behavioral syndromes, extrapair paternity, fitness landscapes, mating preferences, operational sex ratio, reproductive success, sexual selection, temperament. [Behav Ecol]

Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia)

The forces driving the evolution of extra-pair reproduction in socially monogamous animals remain widely debated and unresolved. One key hypothesis is that female extra-pair reproduction evolves through indirect genetic benefits, reflecting increased additive genetic value of extra-pair offspring. Such evolution requires that a female's propensity to produce offspring that are sired by an extra-pair male is heritable. However, additive genetic variance and heritability in female extra-pair paternity (EPP) rate have not been quantified, precluding accurate estimation of the force of indirect selection. Sixteen years of comprehensive paternity and pedigree data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) showed significant additive genetic variance and heritability in the proportion of a female's offspring that was sired by an extra-pair male, constituting major components of the genetic architecture required for extra-pair reproduction to evolve through indirect additive genetic benefits. However, estimated heritabilities were moderately small (0.12 and 0.18 on the observed and underlying latent scales, respectively). The force of selection on extra-pair reproduction through indirect additive genetic benefits may consequently be relatively weak. However, the additive genetic variance and non-zero heritability observed in female EPP rate allow for multiple further genetic mechanisms to drive and constrain mating system evolution.

Sperm Length Variation as a Predictor of Extrapair Paternity in Passerine Birds

BackgroundThe rate of extrapair paternity is a commonly used index for the risk of sperm competition in birds, but paternity data exist for only a few percent of the approximately 10400 extant species. As paternity analyses require extensive field sampling and costly lab work, species coverage in this field will probably not improve much in the foreseeable future. Recent findings from passerine birds, which constitute the largest avian order (∼5 900 species), suggest that sperm phenotypes carry a signature of sperm competition. Here we examine how well standardized measures of sperm length variation can predict the rate of extrapair paternity in passerine birds.Methodology/Principal FindingsWe collected sperm samples from 55 passerine species in Canada and Europe for which extrapair paternity rates were already available from either the same (n = 24) or a different (n = 31) study population. We measured the total length of individual spermatozoa and found that both the coefficient of between-male variation (CVbm) and within-male variation (CVwm) in sperm length were strong predictors of the rate of extrapair paternity, explaining as much as 65% and 58%, respectively, of the variation in extrapair paternity among species. However, only the CVbm predictor was independent of phylogeny, which implies that it can readily be converted into a currency of extrapair paternity without the need for phylogenetic correction.Conclusion/SignificanceWe propose the CVbm index as an alternative measure to extrapair paternity for passerine birds. Given the ease of sperm extraction from male birds in breeding condition, and a modest number of sampled males required for a robust estimate, this new index holds a great potential for mapping the risk of sperm competition across a wide range of passerine birds.

Molecular evidence for extra-pair paternity and intraspecific brood parasitism in the Black-headed Gull

Social monogamy is common among birds, while genetic monogamy is supposed to be rare. I have investigated the genetic mating system of the Black-headed Gull Larus ridibundus in which, as in seabirds and most other long-lived and socially monogamous birds, extra-pair paternity (EPP) is typically rather infrequent. The parentage of 79 chicks from 30 broods was determined based on the analysis of six microsatellite markers. In this study population, evidence of allelic inconsistencies between putative parents and chicks as a result of both EPP and intraspecific brood parasitism (ISBP) was found in 43% of nests . Extra-pair paternity was detected in 33% (10/30) of broods, and 20% (16/79) of all nestlings were sired by extra-pair males. In addition, 9% (7/79) of chicks out of five nests (17%) were not the offspring of either member of the pair, indicating ISBP. These findings reveal a moderate rate of ISBP and a high rate of EPP in the Black-headed Gull compared with other related species and shows that the Black-headed Gulls successfully participate in extra-pair copulations.

Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra-pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6-day-old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra-pair sires primarily occupied territories neighbouring their extra-pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra-pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.

High Fidelity – No Evidence for Extra-Pair Paternity in Siberian Jays (Perisoreus infaustus)

Extra-pair paternity (EPP) in birds is related to a number of ecological and social factors. For example, it has been found to be positively related with breeding density, negatively with the amount of paternal care and especially high rates have been observed in group-living species. Siberian jays (Perisoreous infaustus) breed at low densities and have extended parental care, which leads to the expectation of low rates of EPP. On the other hand, Siberian jays live in groups which can include also unrelated individuals, and provide opportunities for extra-pair matings. To assess the potential occurrence of EPP in Siberian jays, we analysed a large data pool (n = 1029 offspring) covering ca. 30 years of samples from a Finnish Siberian jay population. Paternities were assigned based on up to 21 polymorphic microsatellite markers with the additional information from field observations. We were unable to find any evidence for occurrence of EPP in this species. Our findings are in line with earlier studies and confirm the generally low rates of EPP in related Corvid species. These results suggest that ecological factors may be more important than social factors (group living) in determining costs and benefits of extra-pair paternity.

Synchrony does not explain extrapair paternity rate variation in northern or southern house wrens

Rates of extrapair paternity (EPP) vary widely among and within bird species, and 2 hypotheses suggest that this variation is driven by variation in breeding synchrony. These hypotheses make contradictory predictions, and each has some support from field studies, but the general relationship between EPP and synchrony remains unclear. We investigated EPP in relation to population-wide and local breeding synchrony in 2 populations of house wrens (Troglodytes aedon)—a migratory northern temperate (New York, USA) and a sedentary southern temperate (Buenos Aires, Argentina) population—that differ in numerous life-history traits. The northern population had significantly higher EPP rates and modestly but significantly higher local breeding synchrony. Population-wide breeding synchrony did not differ between populations. The proportion of extrapair young within a nest was not related to the nest’s population-wide or local synchrony index in either population. These results suggest that across divergent life histories in this species, breeding synchrony does not account for within-population variation in EPP.

Low level of extrapair parentage in wild zebra finches

The captive zebra finch, Taeniopygia guttata, has become one of the key vertebrate model systems for studying a range of behavioural, physiological and neurological phenomena. In particular, this species has played a key role in developing our understanding of sexual selection and sperm competition. In contrast with the large number of studies using domesticated zebra finches, relatively few studies have focused on free-living populations of wild zebra finches. Investigating the incidence of extrapair paternity in zebra finches in the Australian desert, we found a very low level; 1.7% of 316 offspring from four of 80 broods fathered outside the pair bond. These numbers contrast with the high levels of extrapair paternity observed in domesticated aviary populations, and suggest a low level of sperm competition and sexual selection in natural populations. Our finding of such a low rate of extrapair paternity in the wild zebra finch suggests that it is one of the most genetically monogamous of all passerine species and that has important implications for future studies of this model organism in studies of sexual selection and reproductive biology. In addition, we found that 5.4% of 316 offspring were not related to either putative parent and hatched from eggs that had been dumped by intraspecific brood parasites.

Long tails matter in sugarbirds—positively for extrapair but negatively for within-pair fertilization success

Extrapair mating is known to occur in many animals and potentially has a significant influence on reproductive success. Female extrapair mate choice may explain the occurrence of exaggerated ornaments in socially monogamous species, but the influence of ornamentation on extrapair mating success has rarely been investigated experimentally. Cape sugarbirds (Promerops cafer) are socially monogamous, almost always lay 2 egg clutches and have long-term pair bonds often lasting several seasons. However, they also display sexually dimorphic extravagant ornamentation in the form of a long, graduated tail and have one of the highest rates (65% of young) of extrapair paternity recorded in birds. We provide a test of the hypothesis that the ornamented tail is used in mate choice for extrapair partners by conducting an experiment in which tail length was manipulated after social mating but before copulation. This experiment therefore allowed females to respond to the manipulation of male tail length when making a choice of copulation partner but not social mate. We show that the tail length of male sugarbirds has a significant effect on the success of males in gaining extrapair paternity, with long-tailed males obtaining significantly more extrapair young than shorttailed males. However, males with short tails sire a significantly greater proportion of the nestlings in their own nests than longtailed individuals. This result suggests that males may adopt alternative strategies dependent on their ornamentation. Key words: extrapair mating, mate choice, Pomerops cafer, sexual selection, sugarbird, tail ornamentation. [Behav Ecol]

Extra-Pair Mating Tactics and Vocal Behavior of Female Acadian Flycatchers

Abstract. In many passerines, rates of extra-pair paternity are high, but relatively few studies have examined the behaviors females use to obtain extra-pair copulations. We studied extra-pair behavior in females of the Acadian Flycatcher (Empidonax virescens), a species in which 58% of females produce extra-pair young and males often sire offspring on distant territories. We used radiotelemetry to document the extent and frequency of females' forays away from their territories and used behavioral observations and playback experiments to test if females' vocalizations advertise their fertility. No radio-tagged females left their territories (n = 12 females, 105 hr of tracking) even during the hour before dawn. Paternity analyses revealed that at least six of these females produced extrapair young. Focal observations revealed that fertile females spent significantly more time calling “chiff,” gave more calls per hour, and called in longer bouts than did incubating females. Extent of females' chiffing durin...

Extra-pair paternity in eastern bluebirds: effects of manipulated density and natural patterns of breeding synchrony

The causes of variation in rates of extra-pair paternity among avian populations remain unclear, but could include environmental factors such as breeding density and synchrony. By experimentally manipulating nest site availability, we tested the effects of breeding density on the frequency of extra-pair paternity in eastern bluebirds (Sialia sialis). We also examined the role of breeding synchrony on extra-pair paternity using natural timing of nests. Microsatellite analysis revealed 34 of 305 nestlings (11.2%) were the result of extra-pair fertilizations; and 21 of 79 broods (26.6%) had at least one extra-pair nestling. Several measures of breeding density had independent effects on extra-pair paternity. First, experimental plot type affected extra-pair paternity, with 28 of 34 (82.4%) extra-pair young from nests in high density areas, and only six (17.6%) from nests in low density areas. Independently of plot type, the number of breeding neighbors within a 320-m radius was a significant predictor of the likelihood of extra-pair paternity at the nest. Extra-pair paternity was associated with temporal factors such as absolute timing of breeding and natural levels of local breeding synchrony, but only in bivariate comparisons. We found a positive interaction between density of neighbors within a 320-m radius and local breeding synchrony; this term reduced the main effects of synchrony and number of neighbors, but not experimental treatment. Our results demonstrate the importance of utilizing multiple aspects of proximity in breeding density analyses and testing for interactions between ecological factors that can influence the behavioral events leading to extra-pair fertilizations.

Short communication: Absence of protandry in a population of Gray Catbirds Dumetella carolinensis

Sex-based differential arrival on the breeding grounds at the completion of migration has been poorly studied in monochromatic and monomorphic species because individuals are difficult to sex without recapture or molecular tests. We examined sex-based arrival timing to the breeding grounds of the Gray Catbird Dumetella carolinensis, a monochromatic species. We also examined differences in size and arrival by age as these are well documented to affect arrival timing. Older birds were larger than younger birds, and older males were larger than older females. Older birds arrived back on the breeding grounds earlier than younger birds, as documented in many species, but males did not precede females. Our results provide evidence of sexual size dimorphism in Catbirds and add to a growing body of information on arrival timing in monochromatic species. Differences in intensity of sex-based competition for breeding resources are hypothesized as the primary selective force for one sex to precede the other to the breeding grounds (Kokko 1999, Kokko et al. 2006). Typically, males arrive at the breeding grounds in advance of females (Morbey & Ydenberg 2001), a phenomenon known as protandry (Rubolini et al. 2004). This is because males are thought to experience more intensive selective pressure for acquiring territories or other resources for attracting a mate than females (but see Kokko et al. 2006 for a discussion of why females may also be under selection pressure for earlier arrival to compete for resources or mates). Furthermore, comparative studies suggest that the extent of sexual selection experienced by males, as evidenced by the degree of sexual dichromatism (Moller & Birkhead 1994, Owens & Hartley 1998), sexual size dimorphism (Owens & Hartley 1998, Dunn et al. 2001), polygyny or rate of extra-pair paternity (Coppack et al. 2006), affects the degree of protandry. While protandry is well documented in dimorphic species (Rubolini et al. 2004), little is known about arrival dates by sex in monomorphic or monochromatic species (Rubolini et al. 2004, Edwards & Forbes 2007, Newton 2008). The primary reason for this is the difficulty in sexing individuals upon arrival at the migratory destination. Moreover, the limited studies to date have produced equivocal results. For example, male Spotted Flycatchers Muscicapa striata preceded females during passage on the island of Ventotene, Italy, (Mabey 2002), and male White-throated Sparrows Zonotrichia albicollis and Least Flycatchers Empidonax minimus preceded females during spring migration at Long Point Observatory, Ontario, Canada (Mills 2005). In contrast, Edwards and Forbes (2007) presented evidence that Song Sparrows Melospiza melodia did not exhibit protandry upon arrival at breeding grounds in Ontario. Our research on arrival and breeding in the Gray Catbird afforded us the opportunity to assess arrival timing by sex and age in a songbird migrant described as monochromatic and monomorphic (Cimprich & Moore 1995). One advantage of our study is that we captured birds both during the arrival period and throughout the breeding season, permitting us to determine an individual’s sex and relate it back to when it arrived at breeding grounds in northeastern Pennsylvania. Although there are several hypotheses regarding differences (or lack of differences) in arrival timing between the sexes (Morbey & Ydenberg 2001) here we focus on assessing whether catbirds are indeed monomorphic and whether they exhibit protandry.

Variation in the extra-pair mating systems of Acadian Flycatchers and Wood Thrushes in forest fragments in southern Ontario

The application of molecular tools to studies of avian mating systems has revealed that most songbird species engage in extra-pair matings. However, little is known about the possible effects of habitat fragmentation on extra-pair mating systems. During the breeding seasons of 2002 and 2003, we quantified the frequency of extra-pair matings in Acadian Flycatchers (Empidonax virescens) and Wood Thrushes (Hylocichla mustelina) nesting in forest fragments in southern Ontario. Acadian Flycatchers are at the limit of their northern range in southern Ontario and occurred at low densities (0.005-0.015 males/ha). Across forest fragments, 14% of young Acadian Flycatchers were the result of extra-pair fertilizations. In contrast, Wood Thrushes were common in forest fragments, with breeding densities ranging from 0.37 to 1 males/ha. Extra-pair mating was common among Wood Thrushes, with 40% of young the result of extra-pair matings. Compared to populations studied in less fragmented habitats in Pennsylvania, rates of extra-pair paternity in Ontario were lower for Acadian Flycatchers and higher for Wood Thrushes. Our results demonstrate that rates of extra-pair mating can vary across landscapes. However, the extra-pair mating systems of Acadian Flycatchers and Wood Thrushes appear to respond differently to fragmentation. We suggest that low breeding densities on fragments may be mediating the low rates of extra-pair mating observed in Acadian Flycatchers in southern Ontario, whereas changes to the behavioral tactics of male and female Wood Thrushes in southern Ontario may explain the high levels of extra-pair mating.

Social structure influences extra-pair paternity in socially monogamous mammals

Using the genetic estimates of paternity available for 22 species of socially monogamous mammals, we investigated the impact of the social structure and of the type of pair bonding on the interspecific variations of extra-pair paternity rates. To this purpose, we classified species in three categories of social structure-solitary, pair or family-living species-and in two categories of pair bonding-intermittent or continuous. We show that interspecific variations of extra-pair paternity rates are better explained by the social structure than by the type of pair bonding. Species with intermittent and continuous pair bonding present similar rates of extra-pair paternity, while solitary and family-living species present higher extra-pair paternity rates than pair-living species. This can be explained by both higher male-male competition and higher female mate choice opportunities in solitary and family-living species than in pair-living species.